Large-scale organization of the hand action observation network in individuals born without handsAugust 28, 2018

​The human high-level visual cortex comprises regions specialized for the processing of distinct types of stimuli, such as objects, animals, and human actions. How does this specialization emerge? Here, we investigated the role of sensorimotor experience in shaping the organization of the action observation network as a window on this question. Observed body movements are frequently coupled with corresponding motor codes, e.g. during monitoring one’s own movements and imitation, resulting in bidirectionally connected circuits between areas involved in body movements observation (e.g., of the hand) and the motor codes involved in their execution. If the organization of the action observation network is shaped by this sensorimotor coupling, then, it should not form for body movements that do not belong to individuals’ motor repertoire. To test this prediction, we used fMRI to investigate the spatial arrangement and functional properties of the hand and foot action observation circuits in individuals born without upper limbs. Multivoxel pattern decoding, pattern similarity, and univariate analyses revealed an intact hand action observation network in the individuals born without upper limbs. This suggests that the organization of the action observation network does not require effector-specific visuomotor coupling.

Plasticity based on compensatory effector use in the association but not primary sensorimotor cortex of people born without handsJuly 11, 2018

Proceedings of the National Academy of Sciences of the U.S.AElla Striem-Amit, Gilles Vannuscorps, & Alfonso Caramazza

What forces direct brain organization and its plasticity? When brain regions are deprived of their input, which regions reorganize based on compensation for the disability and experience, and which regions show topographically constrained plasticity? People born without hands activate their primary sensorimotor hand region while moving body parts used to compensate for this disability (e.g., their feet). This was taken to suggest a neural organization based on functions, such as performing manual-like dexterous actions, rather than on body parts, in primary sensorimotor cortex. We tested the selectivity for the compensatory body parts in the primary and association sensorimotor cortex of people born without hands (dysplasic individuals). Despite clear compensatory foot use, the primary sensorimotor hand area in the dysplasic subjects showed preference for adjacent body parts that are not compensatorily used as effectors. This suggests that function-based organization, proposed for congenital blindness and deafness, does not apply to the primary sensorimotor cortex deprivation in dysplasia. These findings stress the roles of neuroanatomical constraints like topographical proximity and connectivity in determining the functional development of primary cortex even in extreme, congenital deprivation. In contrast, increased and selective foot movement preference was found in dysplasics’ association cortex in the inferior parietal lobule. This suggests that the typical motor selectivity of this region for manual actions may correspond to high-level action representations that are effector-invariant. These findings reveal limitations to compensatory plasticity and experience in modifying brain organization of early topographical cortex compared with association cortices driven by function-based organization.​

Laura obtains an FNRS grant to do her Ph.D. in the lab !! July 2018

Antoine obtains a teaching assistant mandate at UCLouvain and will start a Ph.D. in the lab :-)July 2018

Large-scale organization of the hand action observation network in individuals born without handsApril 23, 2018

​The human high-level visual cortex comprises regions specialized for the processing of distinct types of stimuli, such as objects, animals, and human actions. How does this specialization emerge? Here, we investigated the role of sensorimotor experience in shaping the organization of the action observation network as a window on this question. Observed body movements are frequently coupled with corresponding motor codes, e.g. during monitoring one’s own movements and imitation, resulting in bidirectionally connected circuits between areas involved in body movements observation (e.g., of the hand) and the motor codes involved in their execution. If the organization of the action observation network is shaped by this sensorimotor coupling, then, it should not form for body movements that do not belong to individuals’ motor repertoire. To test this prediction, we used fMRI to investigate the spatial arrangement and functional properties of the hand and foot action observation circuits in individuals born without upper limbs. Multivoxel pattern decoding, pattern similarity, and univariate analyses revealed an intact hand action observation network in the individuals born without upper limbs. This suggests that the organization of the action observation network does not require effector-specific visuomotor coupling.

What forces direct brain organization and its plasticity? When a brain region is deprived of its input would this region reorganize based on compensation for the disability and experience, or would strong limitations of brain structure limit its plasticity? People born without hands activate their sensorimotor hand region while moving body parts used to compensate for this ability (e.g. their feet). This has been taken to suggest a neural organization based on functions, such as performing manual-like dexterous actions, rather than on body parts. Here we test the selectivity for functionally-compensatory body parts in the sensorimotor cortex of people born without hands. Despite clear compensatory foot use, the sensorimotor hand area in the dysplasic subjects showed preference for body parts whose cortical territory is close to the hand area, but which are not compensatorily used as effectors. This suggests that function-based organization, originally proposed for congenital blindness and deafness, does not apply to cases of the primary sensorimotor cortex deprivation in dysplasia. This is consistent with the idea that experience-independent functional specialization occurs at relatively high levels of representation. Indeed, increased and selective foot movement preference in the dysplasics was found in the association cortex, in the inferior parietal lobule. Furthermore, it stresses the roles of neuroanatomical constraints such as topographical proximity and connectivity in determining the functional development of brain regions. These findings reveal limitations to brain plasticity and to the role of experience in shaping the functional organization of the brain.

In everyday actions, we grasp dozens of different manipulable objects in ways that accommodate their functional use. Neuroimaging studies showed that grasping objects in a way that is appropriate for their use involves a left-lateralized network including the supramarginal gyrus (SMG), the anterior intraparietal area (AIP) and the ventral premotor cortex (PMv). However, because previous works premised their conclusions on tasks requiring action execution, it has remained difficult to discriminate between the areas involved in specifying the position of fingers onto the object from those implementing the motor program required to perform the action. To address this issue, we asked healthy participants to make judgements about pictures of manipulable objects while repetitive transcranial magnetic stimulation (rTMS) was applied over the left SMG, AIP, PMv or, as a control, the Vertex. The participants were asked to name the part of the image where the thumb or the index finger was expected to contact the object during its normal utilization or where a given attribute of the same object was located. The two tasks were strictly identical in terms of visual display, working memory demands, and response requirements. Results showed that rTMS over SMG slowed down judgements about finger positioning but not judgements about object attributes. Both types of judgements remained unaffected when rTMS was applied over AIP or PMv. This finding demonstrates that, within the parieto-frontal network dedicated to object use, at least the left SMG is involved in specifying the appropriate position of the thumb and index finger onto the object. ​

Amélie Van Thorre joins the lab :-)September 15, 2017

Amélie has been hired as a teaching assistant in the department and will be the first Ph.D student of the lab :-)She will teach topics related to peripheral and central aspects of typical and atypical speech production, including diagnosis and rehabilitation, in the speech and language therapy program. Her main topic of research will be the causal mechanisms of stuttering. Her main approach will be the neuropsychological study of single-individuals who stutter.

Gilles arrives at UCLouvainAugust 2017

Gilles leaves Cambridge where he was a post-doc in Alfonso Caramazza's lab

Sensorimotor-independent development of hands and tools selectivity in the visual cortex.May 2, 2017

The visual ventral occipital temporal cortex (VOTC) is composed of several distinct regions specialized in the identification of different object kinds such as tools and bodies. Its organization appears to reflect not only the visual characteristics of the inputs but also the behavior that can be achieved with them. For example, there are spatially overlapping responses for viewing hands and tools, which are likely due to their common role in object-directed actions. How dependent is LOTC organization on object manipulation and motor experience? To investigate this question, we studied five individuals born without hands (individuals with upper limb dysplasia; IDs), who use tools with their feet. Using fMRI, we found the typical selective hand-tool overlap (HTO) not only in typically-developed control participants, but also in four of the five IDs. Functional connectivity of the HTO in the IDs also showed a largely similar pattern as in the controls. The clear preservation of functional organization in the IDs suggests that LOTC specialization is driven largely by inherited connectivity constraints that do not require sensorimotor experience. These findings complement discoveries of intact functional LOTC organization in people born blind, supporting an organization largely independent from any one specific sensory or motor experience.

When watching someone reaching to grasp an object, we typically gaze at the object before the agent’s hand reaches it, that is, we make a “predictive eye movement” to the object. The received explanation is that predictive eye movements rely on a direct matching process by which the observed action is mapped onto the motor representation of the same body movements in the observer’s brain. In this paper, we report evidence that calls for a re-examination of this account. We recorded the eye movements of an individual born without arms (D.C.) when watching an actor reaching for one of two different-sized objects with a power grasp, a precision grasp or a closed fist. D.C. showed typical predictive eye movements modulated by the actor’s hand shape. This finding constitutes existence proof that predictive eye movements during action observation can rely on visual and inferential processes unaided by effector-specific motor simulation.

Impaired short-term memory for hand postures in individuals born without hands.July 29, 2016

Cortex, 83, 136-138Gilles Vannuscorps & Alfonso Caramazza

The psychological and neurobiological processes underlying short-term memory for words and objects have been the focus of very numerous studies and of detailed hypotheses (Baddeley, Eysenck & Anderson, 2014; D’Esposito & Postle, 2015). In contrast, the mechanisms that support the temporary storage of information about other’s actions and body postures in memory remain largely unknown. This study focused on a specific issue related to this question: does short-term memory for body postures rely, at least partly, on imitative motoric processes? We compared the performance of seven individuals born with absent or severely shortened upper limbs and no history of phantom limb sensations (IDs; 5 women; mean age = 40.28), and of 19 typically developed control participants (11 women; mean age = 50.64) in a task measuring visual short-term memory for hand postures and in a task measuring visual short-term memory for non-biological patterns.​ The results were in line with the hypothesis that imitative motoric processes can support short term memory for body postures: the individuals born without upper limbs have difficulty in keeping pictures of hand postures in memory even for a short duration

The origin of the biomechanical bias in apparent body movement perceptionMay 27, 2016

Neuropsychologia, 89, 281-286Gilles Vannuscorps & Alfonso Caramazza

The perception of apparent body movement sometimes follows biologically plausible paths rather than paths along the shortest distance as in the case for inanimate objects. For numerous authors, this demonstrates that the somatosensory and motor representations of the observer’s own body support and constrain the perception of others’ body movements. In this paper, we report evidence that calls for a re-examination of this account. We presented an apparent upper limb movement perception task to typically developed participants and five individuals born without upper limbs who were, therefore, totally deprived of somatosensory or motor representations of those limbs. Like the typically developed participants, they showed the typical bias toward long and biomechanically plausible path. This finding suggests that the computations underlying the biomechanical bias in apparent body movement perception is intrinsic to the visual system.

In this study, we addressed the issue of whether the brain sensorimotor circuitry that controls action production is causally involved in representing and processing action-related concepts. We examined the three-year pattern of evolution of brain atrophy, action production disorders, and action-related concept processing in a patient (J.R.) diagnosed with corticobasal degeneration. During the period of investigation, J.R. presented with increasing action production disorders resulting from increasing bilateral atrophy in cortical and subcortical regions involved in the sensorimotor control of actions (notably, the superior parietal cortex, the primary motor and premotor cortex, the inferior frontal gyrus, and the basal ganglia). In contrast, the patient’s performance in processing action-related concepts remained intact during the same period. This finding indicated that action concept processing hinges on cognitive and neural resources that are mostly distinct from those underlying the sensorimotor control of actions

Proceedings of the National Academy of Sciences of the U.S.A, 113, 86-91Gilles Vannuscorps & Alfonso Caramazza

Every day, we interact with people synchronously, immediately understand what they are doing, and easily infer their mental state and the likely outcome of their actions from their kinematics. According to various Motor Simulation Theories of Perception, such efficient perceptual processing of others’ actions cannot be achieved by visual analysis of the movements alone but requires a process of “motor simulation” – an unconscious covert imitation of the observed movements. On this hypothesis, individuals incapable of simulating observed movements in their motor system should have difficulty perceiving and interpreting observed actions. Contrary to this prediction, we found across eight sensitive experiments that individuals born with absent or severely shortened upper limbs (upper limb Dysplasia), despite some variability, could perceive, anticipate, predict, comprehend and memorize upper limb actions, which they cannot simulate, as efficiently as typically developed participants. We also found that, like the typically developed participants, the dysplasic participants systematically perceived the position of moving upper limbs slightly ahead of their real position but only when the anticipated position was not biomechanically awkward. Such anticipatory bias and its modulation by implicit knowledge of the body biomechanical constraints were previously considered as indexes of the crucial role of motor simulation in action perception. Our findings undermine this assumption and the theories that place the locus of action perception and comprehension in the motor system, and invite a shift in the focus of future research to the question of how the visuo-perceptual system represents and processes observed body movements and actions.

Cortex, 67, 147-150Gilles Vannuscorps & Alfonso Caramazza

There is compelling evidence that our perception of others’ bodies and movements is shaped by several rules and constraints, such as the biomechanics of body movement, originally thought to affect only the control and execution of actual movements. For numerous authors, this demonstrates that the perception of others’ bodies and movements is supported by somatosensory and motor representations of our own body. Accordingly, the presence or absence of effects of body constraints on body perception is increasingly used as an index of, respectively, the integrity or impairment of covert stages of action production in patients with motor execution disabilities. However, these biomechanical constraints biases might simply reflect how the visuo-perceptual system processes and represents human bodies. In favor of this alternative, we found that a person born without upper limbs also showed biomechanical biases when asked to provide perceptual judgments about hand postures.

Motor theories of action comprehension claim that comprehending the meaning of an action performed by a conspecific relies on the perceiver’s own motor representation of the same action. According to this view, whether an action belongs to the motor repertoire of the perceiver should impact the ease by which this action is comprehended. We tested this prediction by assessing the ability of an individual (DC) born without upper limbs to comprehend actions involving hands (e.g., throwing) or other body parts (e.g., jumping). The tests used a range of different visual stimuli differing in the kind of information provided. The results showed that DC was as accurate and fast as control participants in comprehending natural video and photographic presentations of both manual and non-manual actions, as well as pantomimes. However, he was selectively impaired at identifying point-light animations of manual actions. This impairment was not due to a difficulty in processing kinematic information per se. DC was indeed as accurate as control participants in two additional tests requiring a fine-grained analysis of an actor’s arm or whole-body movements. These results challenge motor theories of action comprehension by showing that the visual analysis of body shape and motion provides sufficient input for comprehending observed actions. However, when body shape information is sparsely available, motor involvement becomes critical to interpret observed actions. We suggest that, with natural human movement stimuli, motor representations contribute to action comprehension each time visual information is incomplete or ambiguous.

Is motor knowledge part and parcel of the concept of manipulable artifacts ? Clues from a case of upper limb aplasiaSeptember 23, 2013

The sensory-motor theory of conceptual representations assumes that motor knowledge of how an artifact is manipulated is constitutive of its conceptual representation. Accordingly, if we assume that the richer the conceptual representation of an object is, the easier that object is identified, manipulable artifacts that are associated with motor knowledge should be identified more accurately and/or faster than manipulable artifacts that are not (everything else being equal). In this study, we tested this prediction by investigating the identification of manipulable artifacts in an individual, DC, who was totally deprived of hand motor experience due to upper limb aplasia. This condition prevents him from interacting with most manipulable artifacts, for which he thus has no motor knowledge at all. However, he had motor knowledge for some of them, which he routinely uses with his feet. We contrasted DC’s performance in a timed picture naming task for manipulable artifacts for which he had motor knowledge versus those for which he had no motor knowledge. No detectable advantage on DC’s naming performance was found for artifacts for which he had motor knowledge compared to those for which he did not. This finding suggests that motor knowledge is not part of the concepts of manipulable artifacts.

Effect of biomechanical constraints in the hand laterality judgment task: Where does it come from? November 1, 2012

Several studies have reported that, when subjects have to judge the laterality of rotated hand drawings, their judgment is automatically influenced by the biomechanical constraints of the upper limbs. The prominent account for this effect is that, in order to perform the task, subjects mentally rotate their upper limbs toward the position of the displayed stimulus in a way that is consistent with the biomechanical constraints underlying the actual movement. However, the effect of such biomechanical constraints was also found in the responses of motor-impaired individuals performing the hand laterality judgment (HLJ) task, which seems at odds with the “motor imagery” account for this effect. In this study, we further explored the source of the biomechanical constraint effect by assessing the ability of an individual (DC) with a congenital absence of upper limbs to judge the laterality of rotated hand or foot drawings. We found that DC was as accurate and fast as control participants in judging the laterality of both hand and foot drawings, without any disadvantage for hands when compared to feet. Furthermore, DC’s response latencies (RLs) for hand drawings were influenced by the biomechanical constraints of hand movements in the same way as control participants’ RLs. These results suggest that the effect of biomechanical constraints in the HLJ task is not strictly dependent on “motor imagery” and can arise from the visual processing of body parts being sensitive to such constraints.

A domain-specific system for representing knowledge of both man-made objects and human actions. Evidence from a case with an association of deficits. April 17, 2011

Neuropsychologia, 49, 2321-2341Gilles Vannuscorps & Agnesa Pillon

We report the single-case study of a brain-damaged individual, JJG, presenting with a conceptual deficit and whose knowledge of living things, man-made objects, and actions was assessed. The aim was to seek for empirical evidence pertaining to the issue of how conceptual knowledge of objects, both living things and man-made objects, is related to conceptual knowledge of actions at the functional level. We first found that JJG’s conceptual knowledge of both man-made objects and actions was similarly impaired while his conceptual knowledge of living things was spared as well as his knowledge of unique entities. We then examined whether this pattern of association of a conceptual deficit for both man-made objects and actions could be accounted for, first, by the “sensory/functional” and, second, the “manipulability” account for category-specific conceptual impairments advocated within the Feature-Based-Organization theory of conceptual knowledge organization, by assessing, first, patient’s knowledge of sensory compared to functional features, second, his knowledge of manipulation compared to functional features and, third, his knowledge of manipulable compared to non-manipulable objects and actions. The later assessment also allowed us to evaluate an account for the deficits in terms of failures of simulating the hand movements implied by manipulable objects and manual actions. The findings showed that, contrary to the predictions made by the “sensory/functional”, the “manipulability”, and the “failure-of-simulating” accounts for category-specific conceptual impairments, the patient’s association of deficits for both manmade objects and actions was not associated with a disproportionate impairment of functional compared to sensory knowledge or of manipulation compared to functional knowledge; manipulable items were not more impaired than non-manipulable items either. In the general discussion, we propose to account for the patient’s association of deficits by the hypothesis that concepts whose core property is that of being a mean of achieving a goal – like the concepts of man-made objects and of actions – are learned, represented and processed by a common domain-specific conceptual system, which would have evolved to allow human beings to quickly and efficiently design and understand means to achieve goals and purposes.